Home LiteratureArticle Details
PMID: 20148032 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Rfx6 directs islet formation and insulin production in mice and humans.

Nature ·Vol. 463 ·No. 7282 ·2010-02-11 ·Pages 775-80

Smith SB, Qu HQ, Taleb N, Kishimoto NY, Scheel DW, Lu Y, Patch AM, Grabs R, Wang J, Lynn FC, Miyatsuka T, Mitchell J, Seerke R, Désir J, Vanden Eijnden S, Abramowicz M, Kacet N, Weill J, Renard ME, Gentile M, Hansen I, Dewar K, Hattersley AT, Wang R, Wilson ME, Johnson JD, Polychronakos C, German MS

Abstract

Insulin from the beta-cells of the pancreatic islets of Langerhans controls energy homeostasis in vertebrates, and its deficiency causes diabetes mellitus. During embryonic development, the transcription factor neurogenin 3 (Neurog3) initiates the differentiation of the beta-cells and other islet cell types from pancreatic endoderm, but the genetic program that subsequently completes this differentiation remains incompletely understood. Here we show that the transcription factor Rfx6 directs islet cell differentiation downstream of Neurog3. Mice lacking Rfx6 failed to generate any of the normal islet cell types except for pancreatic-polypeptide-producing cells. In human infants with a similar autosomal recessive syndrome of neonatal diabetes, genetic mapping and subsequent sequencing identified mutations in the human RFX6 gene. These studies demonstrate a unique position for Rfx6 in the hierarchy of factors that coordinate pancreatic islet development in both mice and humans. Rfx6 could prove useful in efforts to generate beta-cells for patients with diabetes.

MeSH Terms
Animals Basic Helix-Loop-Helix Transcription Factors/deficiency,genetics,metabolism Cell Differentiation DNA Mutational Analysis DNA-Binding Proteins/deficiency,genetics,metabolism Diabetes Mellitus/congenital,genetics,metabolism,pathology Embryo, Mammalian/metabolism Female Fetus/metabolism Gene Expression Profiling Gene Expression Regulation, Developmental Genes, Recessive/genetics Genetic Testing Humans Infant, Newborn Insulin/biosynthesis Islets of Langerhans/cytology,embryology,metabolism Male Mice NIH 3T3 Cells Nerve Tissue Proteins/deficiency,genetics,metabolism Organ Specificity Regulatory Factor X Transcription Factors Syndrome Transcription Factors/deficiency,genetics,metabolism
Chemicals
Basic Helix-Loop-Helix Transcription Factors DNA-Binding Proteins Insulin Nerve Tissue Proteins Neurog3 protein, mouse Regulatory Factor X Transcription Factors Rfx6 protein, human Rfx6 protein, mouse Transcription Factors
Authors & Affiliations
28 authors, click to expand affiliations / ORCID
Smith Stuart B
Diabetes Center, University of California San Francisco, San Francisco, California 94143, USA.
Qu Hui-Qi
Taleb Nadine
Kishimoto Nina Y
Scheel David W
Lu Yang
Patch Ann-Marie
Grabs Rosemary
Wang Juehu
Lynn Francis C
Miyatsuka Takeshi
Mitchell John
Seerke Rina
Désir Julie
Vanden Eijnden Serge
Abramowicz Marc
Kacet Nadine
Weill Jacques
Renard Marie-Eve
Gentile Mattia
Hansen Inger
Dewar Ken
Hattersley Andrew T
Wang Rennian
Wilson Maria E
Johnson Jeffrey D
Polychronakos Constantin
German Michael S
References (42)
42 references, click to expand
  1. MicroRNA expression is required for pancreatic islet cell genesis in the mouse.
    Diabetes. 2007 Dec;56(12):2938-45 PMID: 17804764
  2. Transcription factor expression in the developing human fetal endocrine pancreas.
    Diabetologia. 2008 Jul;51(7):1169-80 PMID: 18491072
  3. Learning from molecular genetics: novel insights arising from the definition of genes for monogenic and type 2 diabetes.
    Diabetes. 2008 Nov;57(11):2889-98 PMID: 18971436
  4. Sox9 coordinates a transcriptional network in pancreatic progenitor cells.
    Proc Natl Acad Sci U S A. 2007 Jun 19;104(25):10500-5 PMID: 17563382
  5. Whole genome genotyping technologies on the BeadArray platform.
    Biotechnol J. 2007 Jan;2(1):41-9 PMID: 17225249
  6. Neurogenin 3 is essential for the proper specification of gastric enteroendocrine cells and the maintenance of gastric epithelial cell identity.
    Genes Dev. 2002 Jun 15;16(12):1488-97 PMID: 12080087
  7. The nonsense-mediated decay RNA surveillance pathway.
    Annu Rev Biochem. 2007;76:51-74 PMID: 17352659
  8. A consensus motif in the RFX DNA binding domain and binding domain mutants with altered specificity.
    Mol Cell Biol. 1996 Aug;16(8):4486-94 PMID: 8754849
  9. Independent development of pancreatic alpha- and beta-cells from neurogenin3-expressing precursors: a role for the notch pathway in repression of premature differentiation.
    Diabetes. 2000 Feb;49(2):163-76 PMID: 10868931
  10. A further example of a distinctive autosomal recessive syndrome comprising neonatal diabetes mellitus, intestinal atresias and gall bladder agenesis.
    Am J Med Genet A. 2008 Jul 1;146A(13):1713-7 PMID: 18512226
  11. Novel function of the ciliogenic transcription factor RFX3 in development of the endocrine pancreas.
    Diabetes. 2007 Apr;56(4):950-9 PMID: 17229940
  12. Mutant neurogenin-3 in congenital malabsorptive diarrhea.
    N Engl J Med. 2006 Jul 20;355(3):270-80 PMID: 16855267
  13. Towards a proteome-scale map of the human protein-protein interaction network.
    Nature. 2005 Oct 20;437(7062):1173-8 PMID: 16189514
  14. Primary cilia deletion in pancreatic epithelial cells results in cyst formation and pancreatitis.
    Gastroenterology. 2006 Dec;131(6):1856-69 PMID: 17123526
  15. Genome-wide in situ exon capture for selective resequencing.
    Nat Genet. 2007 Dec;39(12):1522-7 PMID: 17982454
  16. Structure of the winged-helix protein hRFX1 reveals a new mode of DNA binding.
    Nature. 2000 Feb 24;403(6772):916-21 PMID: 10706293
  17. Direct selection of human genomic loci by microarray hybridization.
    Nat Methods. 2007 Nov;4(11):903-5 PMID: 17934467
  18. RFX proteins, a novel family of DNA binding proteins conserved in the eukaryotic kingdom.
    Nucleic Acids Res. 1996 Mar 1;24(5):803-7 PMID: 8600444
  19. Notch signalling controls pancreatic cell differentiation.
    Nature. 1999 Aug 26;400(6747):877-81 PMID: 10476967
  20. A novel susceptibility locus for type 1 diabetes on Chr12q13 identified by a genome-wide association study.
    Diabetes. 2008 Apr;57(4):1143-6 PMID: 18198356
  21. Recombineering: a powerful new tool for mouse functional genomics.
    Nat Rev Genet. 2001 Oct;2(10):769-79 PMID: 11584293
  22. Interaction of EF-C/RFX-1 with the inverted repeat of viral enhancer regions is required for transactivation.
    J Biol Chem. 1995 Apr 7;270(14):8353-60 PMID: 7713944
  23. Direct evidence for the pancreatic lineage: NGN3+ cells are islet progenitors and are distinct from duct progenitors.
    Development. 2002 May;129(10):2447-57 PMID: 11973276
  24. TiGER: a database for tissue-specific gene expression and regulation.
    BMC Bioinformatics. 2008 Jun 09;9:271 PMID: 18541026
  25. Chronology of islet differentiation revealed by temporal cell labeling.
    Diabetes. 2009 Aug;58(8):1863-8 PMID: 19478145
  26. Neonatal diabetes, with hypoplastic pancreas, intestinal atresia and gall bladder hypoplasia: search for the aetiology of a new autosomal recessive syndrome.
    Diabetologia. 2004 Dec;47(12):2160-7 PMID: 15592663
  27. neurogenin3 is required for the development of the four endocrine cell lineages of the pancreas.
    Proc Natl Acad Sci U S A. 2000 Feb 15;97(4):1607-11 PMID: 10677506
  28. The UCSC Genome Browser Database: 2008 update.
    Nucleic Acids Res. 2008 Jan;36(Database issue):D773-9 PMID: 18086701
  29. Induction of pancreatic islet cell differentiation by the neurogenin-neuroD cascade.
    Differentiation. 2008 Apr;76(4):381-91 PMID: 17924961
  30. Signals from the neural crest regulate beta-cell mass in the pancreas.
    Development. 2008 Jun;135(12):2151-60 PMID: 18506029
  31. A quantitative immunofluorescent study of the endocrine cell populations in the developing human pancreas.
    Diabetes. 1983 Apr;32(4):293-301 PMID: 6131849
  32. Orpk mouse model of polycystic kidney disease reveals essential role of primary cilia in pancreatic tissue organization.
    Development. 2004 Jul;131(14):3457-67 PMID: 15226261
  33. Mutant neurogenin-3 in congenital malabsorptive diarrhea.
    N Engl J Med. 2007 Apr 26;356(17):1781-2; author reply 1782 PMID: 17460236
  34. Genome-wide association study of 14,000 cases of seven common diseases and 3,000 shared controls.
    Nature. 2007 Jun 7;447(7145):661-78 PMID: 17554300
  35. Generalized lacZ expression with the ROSA26 Cre reporter strain.
    Nat Genet. 1999 Jan;21(1):70-1 PMID: 9916792
  36. Pancreas and beta-cell development: from the actual to the possible.
    Development. 2007 Feb;134(3):427-38 PMID: 17185316
  37. Identification and characterization of novel human tissue-specific RFX transcription factors.
    BMC Evol Biol. 2008 Aug 01;8:226 PMID: 18673564
  38. A genome-wide association study identifies novel risk loci for type 2 diabetes.
    Nature. 2007 Feb 22;445(7130):881-5 PMID: 17293876
  39. Myt1 and Ngn3 form a feed-forward expression loop to promote endocrine islet cell differentiation.
    Dev Biol. 2008 May 15;317(2):531-40 PMID: 18394599
  40. Expression of neurogenin3 reveals an islet cell precursor population in the pancreas.
    Development. 2000 Aug;127(16):3533-42 PMID: 10903178
  41. Esophageal, duodenal, rectoanal and biliary atresia, intestinal malrotation, malformed/hypoplastic pancreas, and hypospadias: further evidence of a new distinct syndrome.
    Am J Med Genet. 1999 Nov 5;87(1):82-3 PMID: 10528254
  42. Enteroendocrine cell dysgenesis and malabsorption, a histopathologic and immunohistochemical characterization.
    Hum Pathol. 2007 Apr;38(4):570-80 PMID: 17258790
Article Info
Journal
Nature
Abbr.
Nature
ISSN
1476-4687
Published
2010-02-11
Pages
775-80
Language
English
Region
England
NLM ID
0410462
PMCID
PMC2896718
Subset
IM
Grants
NIDDK NIH HHS · U19 DK061245-04 · United States
NIDDK NIH HHS · P30 DK063720-045956 · United States
NIDDK NIH HHS · P30 DK063720 · United States
NIDDK NIH HHS · R01 DK021344 · United States
NIDDK NIH HHS · P30 DK063720-05 · United States
NIDDK NIH HHS · P30 DK063720-045957 · United States
NIDDK NIH HHS · P30 DK063720-045958 · United States
NIDDK NIH HHS · P30 DK063720-045954 · United States
NIDDK NIH HHS · U19 DK061245 · United States
NIDDK NIH HHS · P30 DK063720-045955 · United States
NIDDK NIH HHS · R01 DK021344-26 · United States
NIDDK NIH HHS · U19 DK061245-049001 · United States
CIHR · Canada
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]